Developmental immune history affects adult immune function but not carotenoid‐based ornamentation in mallard ducks

Abstract

Summary1. Sexually selected traits often honestly advertise aspects of individual quality, such as immune function. Such traits have traditionally been thought to reveal real-time information (e.g. current health state), but they may also reflect immunological conditions experienced during ontogeny, which can fundamentally shape survival prospects, adult immune function, and reproductive performance. 2. We tested the effects of immune challenges (injections of sheep red blood cells) during neonatal development on adult immune function and ornamental coloration in male mallard ducks (Anas platyrhynchos). Mallards have a carotenoid-pigmented beak that plays a role in mate choice, and because carotenoids are also associated with immune responsiveness, carotenoid accumulation in body tissues may change as a function of immunological state during development and into adulthood. 3. We found that mallards that received immune challenges at the completion of growth (8-10 weeks old) had a reduced proinflammatory response (as measured by the local swelling response to phytohemagglutinin; PHA) as adults, compared to control birds and those receiving immune challenges at other developmental time points. Mallards that received immune challenges during the acquisition of nuptial plumage (13-15 weeks old) had an increased humoral immune response as adults, as assessed by antibody production to keyhole limpet hemocyanin (KLH). Body mass, adult beak colour, and carotenoid circulation were not affected by immune challenges issued at any point during development. 4. Circulating carotenoid levels prior to adult immune challenge and change in carotenoid titre over the course of the adult immune assessment period were correlated with degree of response to PHA and KLH at adulthood, as well as with nitric oxide production, which is associated with innate immunity. However, the direction of these correlations varied by type of immune assessment. Surprisingly, unlike in several previous studies, we found no link between beak coloration and adult immune function.5. These findings demonstrate the importance of developmental immune challenges in shaping adult immune response, although the precise mechanisms remain unidentified. Moreover, we found support for the hypothesis that carotenoids are linked to immune function, because of the relationship between multiple immune responses and both initial and change in circulating carotenoid levels. 6. However, our study does not support the hypothesis that sexual signal expression reveals developmental immune history. Taken together, our findings suggest that the relationships between carotenoid physiology, carotenoid-based ornamentation, and immune function are complex.

Eggshell coloration reflects both yolk characteristics and dietary carotenoid history of female mallards

“…We acquired 46 one‐day‐old female ducklings from Metzer Farms (Gonzales, CA, USA) in December 2009 and housed them as in Butler & McGraw (, ). Ducklings were reared indoors in randomly selected groups of five ducklings per cage (60 × 60 × 60 cm) until they were 2 weeks old, then three per cage until they were 4 weeks old, and then two per cage until they were 7 weeks old, at which point all birds were moved outside and individually housed to allow for normal sexual maturation (Butler & McGraw , ). Light : dark regime was 13L : 11D when ducklings were housed indoors, and natural photoperiod thereafter (10·5L : 13·5D at 7 weeks old to 13·5L : 10·5D at 20 weeks old).…”

Differential Effects of Early- and Late-Life Access to Carotenoids on Adult Immune Function and Ornamentation in Mallard Ducks (Anas platyrhynchos)

“…We have described these challenges in detail elsewhere [52], [55], so here we briefly review our methodologies.…”

“…We quantified total carotenoid titer (predominately lutein and zeaxanthin; [55]) for all individuals at the beginning and end of DEV, the beginning of ADULT, and on D0, D1, D6, and D10 of the adult immune assessment period.…”

Imperfect past and present progressive: beak color reflects early-life and adult exposure to antigen

“…If CORT can lead to a reduction in beak coloration (sensu McGraw et al 2011), highquality males may have the ability to buffer against increases in circulating CORT. Butler and McGraw (2012b) found that baseline bill saturation in mallards (Anas platyrhynchos) was positively correlated with their cutaneous immune response, although they failed to find a relationship between Ab levels in response to KLH challenge and aspects of bill color or circulating carotenoid levels. Faivre et al (2003) demonstrated that blackbirds (Turdus merula) challenged with sheep red blood cells (SRBCs) exhibited a rapid decline in yellow coloration, but that, in contrast to our findings, the likelihood of becoming duller was positively linked to the strength of anti-SRBC response.…”

“…Faivre et al (2003) demonstrated that blackbirds (Turdus merula) challenged with sheep red blood cells (SRBCs) exhibited a rapid decline in yellow coloration, but that, in contrast to our findings, the likelihood of becoming duller was positively linked to the strength of anti-SRBC response. The yellow coloration of the blackbird and mallard beaks is dependent upon carotenes and zeaxanthins (blackbird: Faivre et al 2003), and xanthophylls and zeaxanthins (mallards (Butler and McGraw 2012b), and is not dependent upon ketocarotenoids as is beak coloration in zebra finches. The yellow beak may represent more basic components of resource acquisition (Hill 2002), rather than processes related to metabolic efficiency (Hill 2014;Ge et al 2015).…”